Skip to main content

Survey of potential factors involved in the low frequency of CP5 and CP8 expression in Staphylococcus aureus isolates from mastitis of dairy cattle from Argentina, Chile, and Uruguay

Journal of Applied Genetics volume 59, pages 357–363 (2018)Cite this article

Abstract

Staphylococcus aureus produces capsular polysaccharides (CPs) both in vivo and under defined culture conditions being serotypes 5 and 8 the most prevalent. S. aureus isolates that fail to produce CP5 or CP8 are defined as non-typeable (NT). Loss of capsule expression, however, may lead to S. aureus persistence in a chronically infected host. The prevalence of NT strains of S. aureus isolated from bovine mastitis varies according to the geographic origin of the strain. The aims of this work were to detect phenotypically and genotypically the capsular profile of 144 S. aureus isolated from bovine mastitis in Argentina, Chile, and Uruguay and explore the factors that are considered to be associated with capsule expression as presence of IS257, IScap, and agr typing of non-related collection. The detection of the IS257, IScap, cap genes, and agr typing was performed using PCR. The detection and quantification of capsular polysaccharide production were performed by ELISA assays. We found that 96% of the S. aureus isolates investigated carried cap5(8) genes but over 75% of strains do not express capsule in the three countries studied. However, only 6 isolates from Argentina carried the IScap element that totally suppressed the expression of the capsule, suggesting that other factors could influence on CP expression. Moreover, the agrI/NT association was statistically significant suggesting that this profile is a phenomenon observed not only in other parts of the world but also in our region.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  • Bardiau M, Detilleux J, Farnir F, Mainil JG, Ote I (2014) Associations between properties linked with persistence in a collection of Staphylococcus aureus isolates from bovine mastitis. Vet Microbiol 169:74–79

    Article  PubMed  Google Scholar 

  • Bardiau M, Caplin J, Detilleux J, Graber H, Moroni P, Taminiau B, Mainil JG (2016) Existence of two groups of Staphylococcus aureus strains isolated from bovine mastitis based on biofilm formation, intracellular survival, capsular profile and agr-typing. Vet Microbiol 185:1–6

    Article  PubMed  CAS  Google Scholar 

  • Boyle-Vavra S et al (2015) USA300 and USA500 clonal lineages of Staphylococcus aureus do not produce a capsular polysaccharide due to conserved mutations in the cap5 locus. MBio 6:02585–02514

    Article  CAS  Google Scholar 

  • Buzzola FR, Alvarez LP, Tuchscherr LP, Barbagelata MS, Lattar SM, Calvinho L, Sordelli DO (2007) Differential abilities of capsulated and noncapsulated Staphylococcus aureus isolates from diverse agr groups to invade mammary epithelial cells. Infect Immun 75:886–891

    Article  PubMed  CAS  Google Scholar 

  • Camussone C, Rejf P, Pujato N, Schwab A, Marcipar I, Calvinho LF (2012) Genotypic and phenotypic detection of capsular polysaccharides in Staphylococcus aureus isolated from bovine intramammary infections in Argentina. Braz J Microbiol 43:1010–1014

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chandler M, Mahillon J (2002) Insertion sequences revisited. In: Craig NL, Craigie R, Gellert M, Lambovitz AM (eds) Mobile DNA II. ASM Press, Washington, DC, pp 305–366

    Chapter  Google Scholar 

  • Cheng BL et al (2017) Evaluation of serotypes 5 and 8 capsular polysaccharides in protection against Staphylococcus aureus in murine models of infection. Hum Vaccin Immunother 13:1609–1614

    Article  PubMed  PubMed Central  Google Scholar 

  • Cocchiaro JL, Gomez MI, Risley A, Solinga R, Sordelli DO, Lee JC (2006) Molecular characterization of the capsule locus from non-typeable Staphylococcus aureus. Mol Microbiol 59:948–960

    Article  PubMed  CAS  Google Scholar 

  • Cunnion K, Zhang H, Frank M (2003) Availability of complement bound to Staphylococcus aureus to interact with membrane complement receptors influences efficiency of phagocytosis. Infect Immun 71:656–662

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Firth N, Skurray RA (2006) Genetics: accessory elements and genetic exchange. In: Fischetti VA, Novick RP, Ferretti JR, Portnoy DA, Rood JI (eds) Gram-positive pathogens, 2nd edn. ASM Press, Washington, DC, pp 413–426

    Chapter  Google Scholar 

  • Gilot P, Lina G, Cochard T, Poutrel B (2002) Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a population of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol 40:4060–4067

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guidry AJ, Oliver SP, Squiggins KE, Erbe EF, Dowlen HH, Hambleton CN, Berning LM (1991) Effect of anticapsular antibodies on neutrophil phagocytosis of Staphylococcus aureus. J Dairy Sci 74:3360–3369

    Article  PubMed  CAS  Google Scholar 

  • Guidry A, Fattom A, Patel A, O'Brien C (1997) Prevalence of capsular serotypes among Staphylococcus aureus isolates from cows with mastitis in the United States. Vet Microbiol 59:53–58

    Article  PubMed  CAS  Google Scholar 

  • Han HR, Pak S 2nd, Guidry A (2000) Prevalence of capsular polysaccharide (CP) types of Staphylococcus aureus isolated from bovine mastitic milk and protection of S. aureus infection in mice with CP vaccine. J Vet Med Sci 62:1331–1333

    Article  PubMed  CAS  Google Scholar 

  • Hata E, Katsuda K, Kobayashi H, Ogawa T, Endo T, Eguchi M (2006) Characteristics and epidemiologic genotyping of Staphylococcus aureus isolates from bovine mastitic milk in Hokkaido, Japan. J Vet Med Sci 68:165–170

    Article  PubMed  CAS  Google Scholar 

  • Karakawa WW, Vann WF (1982) Capsular polysaccharides of Staphylococcus aureus Semin Infect Dis 2:285–293

  • Karakawa WW, Fournier JM, Vann WF, Arbeit R, Schneerson RS, Robbins JB (1985) Method for the serological typing of the capsular polysaccharides of Staphylococcus aureus. J Clin Microbiol 22:445–447

    PubMed  PubMed Central  CAS  Google Scholar 

  • Khichar V, Kataria AK (2014) Capsular genotyping (cap5k and cap8k) of Staphylococcus aureus isolates from cattle with clinical mastitis. Human & Veterinary Medicine international journal bioflux society 6(1):30–33

  • Lawrence JG, Ochman H, Hartl DL (1992) The evolution of insertion sequences within enteric bacteria. Genetics 131:9–20

    PubMed  PubMed Central  CAS  Google Scholar 

  • Lee CY, Lee JC (2006) Staphylococcal capsule. In: Fischetti VA, Novick RP, Ferretti JJ, Portnoy DA, Rood JI (eds) Gram-positive pathogens. 2nd edn. ASM Press, Washington, DC., pp 456–463

  • Lee J, Takeda S, Livolsi P, Paoletti L (1993) Effects of in vitro and in vivo growth conditions on expression of type 8 capsular polysaccharide by Staphylococcus aureus. Infect Immun 61:1853–1858

    PubMed  PubMed Central  CAS  Google Scholar 

  • Martineau F, Picard FJ, Roy PH, Ouellette M, Bergeron MG (1998) Species-specific and ubiquitous-DNA-based assays for rapid identification of Staphylococcus aureus. J Clin Microbiol 36:618–623

    PubMed  PubMed Central  CAS  Google Scholar 

  • O’Riordan K, Lee JC (2004) Staphylococcus aureus capsular polysaccharide. Clin Microbiol Rev 17:218–234

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304

    Article  PubMed  CAS  Google Scholar 

  • Pitcher D, Saunders N, Owen R (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8:151–156

    Article  CAS  Google Scholar 

  • Pohlmann-Dietze P et al (2000) Adherence of Staphylococcus aureus to endothelial cells: influence of capsular polysaccharide, global regulator agr, and bacterial growth phase. Infect Immun 68:4865–4871

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Poutrel B, Boutonnier A, Sutra L, Fournier JM (1988) Prevalence of capsular polysaccharide types 5 and 8 among Staphylococcus aureus isolates from cow, goat, and ewe milk. J Clin Microbiol 26:38–40

    PubMed  PubMed Central  CAS  Google Scholar 

  • Quelle LS, Corso A, Galas M, Sordelli DO (2003) STAR gene restriction profile analysis in epidemiological typing of methicillin-resistant Staphylococcus aureus: description of the new method and comparison with other polymerase chain reaction (PCR)-based methods. Diagn Microbiol Infect Dis 47:455–464

    Article  PubMed  CAS  Google Scholar 

  • Salimena AP et al (2016) Genotypic and phenotypic detection of capsular polysaccharide and biofilm formation in Staphylococcus aureus isolated from bovine milk collected from Brazilian dairy farms. Vet Res Commun 40:97–106

    Article  PubMed  Google Scholar 

  • Simpson AE, Skurray RA, Firth N (2000) An IS257-derived hybrid promoter directs transcription of a tetA(K) tetracycline resistance gene in the Staphylococcus aureus chromosomal mec region. J Bacteriol 182:3345–3352

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sordelli DO et al (2000) Capsule expression by bovine isolates of Staphylococcus aureus from Argentina: genetic and epidemiologic analyses. J Clin Microbiol 38:846–850

    PubMed  PubMed Central  CAS  Google Scholar 

  • Stringfellow W, Dassy B, Lieb M, Fournier JM (1991) Staphylococcus aureus growth and type 5 capsular polysaccharide production in synthetic media. Appl Environ Microbiol 57:618–621

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sutra L, Poutrel B (1994) Virulence factors involved in the pathogenesis of bovine intramammary infections due to Staphylococcus aureus. J Med Microbiol 40:79–89

    Article  PubMed  CAS  Google Scholar 

  • Tenover FC, Arbeit RD, Goering RV, Mickelsen PA, Murray BE, Persing DH, and Swaminathan B (1995) Interpreting chromosomal DNA restriction patternsproduced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol 33:2233–2239

  • Tollersrud T, Kenny K, Reitz AJJ, Lee JC (2000) Genetic and serologic evaluation of capsule production by bovine mammary isolates of Staphylococcus aureus and other Staphylococcus spp. from Europe and the United States J Clin Microbiol 38 (8):2998–3003

  • Tollersrud T, Zernichow L, Andersen SR, Kenny K, Lund A (2001) Staphylococcus aureus capsular polysaccharide type 5 conjugate and whole cell vaccines stimulate antibody responses in cattle. Vaccine 19:3896–3903

    Article  PubMed  CAS  Google Scholar 

  • Tuchscherr LPN, Buzzola FR, Alvarez LP, Caccuri RL, Lee JC, Sordelli DO (2005) Capsule-negative Staphylococcus aureus induces chronic experimental mastitis in mice. Infect Immun 73:7932–7937

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tuchscherr LP, Gomez MI, Buzzola FR, Calvinho LF, Lee JC, Sordelli DO (2007) Characterization of a new variant of IS257 that has displaced the capsule genes within bovine isolates of Staphylococcus aureus. Infect Immun 75:5483–5488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van de Peer Y, De Wachter R (1994) TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10:569–570

    PubMed  Google Scholar 

  • Verdier I et al (2007) Identification of the capsular polysaccharides in Staphylococcus aureus clinical isolates by PCR and agglutination tests. J Clin Microbiol 45:725–729

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu S, Arbeit R, Lee J (1992) Phagocytic killing of encapsulated and microencapsulated Staphylococcus aureus by human polymorphonuclear leukocytes. Infect Immun 60:1358–1362

Download references

Funding

M.S.P. was a fellow from CONICET, and I.S.M. and C. C. are independent and assistant members of the research career of CONICET. This work was supported by grants from FONCyT (M.S.B., PICT Bicentenario 2010-1309), (L.F.C. and I.S.M., PICT 1175) and from Fundación Banco de la Provincia de Santa Fe (M.S.B.)

Author information

Authors and Affiliations

  1. Laboratorio de Tecnología Inmunológica, Facultad de Bioquímica y Ciencias Biológicas, Universidad Nacional del Litoral, Ciudad Universitaria, RN168, 3000, Santa Fe, Argentina

    Maria Belen Ambroggio, Melina Soledad Perrig, Nazarena Pujato, Ivan Sergio Marcipar & Maria Sol Barbagelata

  2. Estación Experimental Agropecuaria Rafaela, Instituto Nacional de Tecnología Agropecuaria (INTA), Rafaela, Santa Fe, Argentina

    Cecilia Camussone & Luis Fernando Calvinho

  3. Consejo Nacional de Investigaciones Científicas y Técnicas, CONICET, Buenos Aires, Argentina

    Cecilia Camussone & Ivan Sergio Marcipar

  4. Colonia Cosmopolita, Departamento de Colonia, Lactodiagnóstico Sur Uruguay, Colonia del Sacramento, Uruguay

    Alicia Bertón

  5. Laboratory Veterinary Direction “Miguel C. Rubino”, Paysandú, Uruguay

    Edgardo Gianneechini

  6. Udder Health, Osorno, X Región, Chile

    Silvia Alvarez

  7. Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral, Santa Fe, Argentina

    Luis Fernando Calvinho

Authors
  1. Maria Belen Ambroggio
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Melina Soledad Perrig
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cecilia Camussone
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nazarena Pujato
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alicia Bertón
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Edgardo Gianneechini
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Silvia Alvarez
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ivan Sergio Marcipar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Luis Fernando Calvinho
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Maria Sol Barbagelata
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maria Sol Barbagelata.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by: Agnieszka Szalewska-Palasz

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ambroggio, M.B., Perrig, M.S., Camussone, C. et al. Survey of potential factors involved in the low frequency of CP5 and CP8 expression in Staphylococcus aureus isolates from mastitis of dairy cattle from Argentina, Chile, and Uruguay. J Appl Genetics 59, 357–363 (2018). https://doi.org/10.1007/s13353-018-0443-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13353-018-0443-8

Keywords

  • Staphylococcus aureus
  • Capsule expression
  • IScap
  • agr typing
  • Bovine mastitis